Oxytocin enhances cranial visceral afferent synaptic transmission to the solitary tract nucleus

James H. Peters, Stuart J. McDougall, Daniel O. Kellett, David Jordan, Ida J. Llewellyn-Smith, Michael Andresen

Research output: Contribution to journalArticle

87 Citations (Scopus)

Abstract

Cranial visceral afferents travel via the solitary tract (ST) to contact neurons within the ST nucleus (NTS) and activate homeostatic reflexes. Hypothalamic projections from the paraventricular nucleus (PVN) release oxytocin (OT) to modulate visceral afferent communication with NTS neurons. However, the cellular mechanisms through which OT acts are poorly understood. Here, we electrophysiologically identified second-order NTS neurons in horizontal brainstem slices by their low-jitter, ST-evoked glutamatergic EPSCs. OT increased the frequency of miniature EPSCs in half of the NTS second-order neurons (13/24) but did not alter event kinetics or amplitudes. These actions were blocked by a selective OT receptor antagonist. OT increased the amplitude of ST-evoked EPSCs with no effect on event kinetics. Variance-mean analysis of ST-evoked EPSCs indicated OT selectively increased the release probability of glutamate from the ST afferent terminals. In OT-sensitive neurons, OT evoked an inward holding current and increased input resistance. The OT-sensitive current reversed at the K+ equilibrium potential. In in vivo studies, NTS neurons excited by vagal cardiopulmonary afferents were juxtacellularly labeled with Neurobiotin and sections were stained to show filled neurons and OT-immunoreactive axons. Half of these physiologically characterized neurons (5/10) showed close appositions by OT fibers consistent with synaptic contacts. Electron microscopy of medial NTS found immunoreactive OT within synaptic boutons. Together, these findings suggest that OT released from PVN axons acts on a subset of second-order neurons within medial NTS to enhance visceral afferent transmission via presynaptic and postsynaptic mechanisms.

Original languageEnglish (US)
Pages (from-to)11731-11740
Number of pages10
JournalJournal of Neuroscience
Volume28
Issue number45
DOIs
StatePublished - Nov 5 2008

Fingerprint

Visceral Afferents
Solitary Nucleus
Oxytocin
Synaptic Transmission
Neurons
Paraventricular Hypothalamic Nucleus
Axons
Oxytocin Receptors
Presynaptic Terminals
Brain Stem

Keywords

  • Autonomic
  • Brainstem
  • Immunocytochemistry
  • Synaptic
  • Ultrastructure
  • Vagal afferents

ASJC Scopus subject areas

  • Neuroscience(all)

Cite this

Oxytocin enhances cranial visceral afferent synaptic transmission to the solitary tract nucleus. / Peters, James H.; McDougall, Stuart J.; Kellett, Daniel O.; Jordan, David; Llewellyn-Smith, Ida J.; Andresen, Michael.

In: Journal of Neuroscience, Vol. 28, No. 45, 05.11.2008, p. 11731-11740.

Research output: Contribution to journalArticle

Peters, James H. ; McDougall, Stuart J. ; Kellett, Daniel O. ; Jordan, David ; Llewellyn-Smith, Ida J. ; Andresen, Michael. / Oxytocin enhances cranial visceral afferent synaptic transmission to the solitary tract nucleus. In: Journal of Neuroscience. 2008 ; Vol. 28, No. 45. pp. 11731-11740.
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